Control of breathing and adaptation to high altitude in the bar-headed goose

Scott, Graham R.; Milsom, William K.

doi:10.1152/ajpregu.00161.2007

Cited by 96 publications

(117 citation statements)

References 62 publications

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“…Instead, these results suggest a primary reliance on lipid catabolism during steady-state thermogenesis. The decline in RER appeared to be more gradual in the highland deer mice, but this result is difficult to interpret, as it may reflect an increased rate of carbohydrate oxidation at the onset of thermogenesis or ventilatory hypocapnia due to an enhanced hypoxic ventilatory response in highland deer mice (37,38). Nonetheless, all of the mice were apparently relying almost exclusively on lipid oxidation after 10 min of sustained thermogenesis ( Fig.…”

Section: Resultsmentioning

confidence: 94%

Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice

Cheviron

Bachman

Connaty

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

168

226

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In response to hypoxic stress, many animals compensate for a reduced cellular O 2 supply by suppressing total metabolism, thereby reducing O 2 demand. For small endotherms that are native to high-altitude environments, this is not always a viable strategy, as the capacity for sustained aerobic thermogenesis is critical for survival during periods of prolonged cold stress. For example, survivorship studies of deer mice (Peromyscus maniculatus) have demonstrated that thermogenic capacity is under strong directional selection at high altitude. Here, we integrate measures of whole-organism thermogenic performance with measures of metabolic enzyme activities and genomic transcriptional profiles to examine the mechanistic underpinnings of adaptive variation in this complex trait in deer mice that are native to different elevations. We demonstrate that highland deer mice have an enhanced thermogenic capacity under hypoxia compared with lowland conspecifics and a closely related lowland species, Peromyscus leucopus. Our findings suggest that the enhanced thermogenic performance of highland deer mice is largely attributable to an increased capacity to oxidize lipids as a primary metabolic fuel source. This enhanced capacity for aerobic thermogenesis is associated with elevated activities of muscle metabolic enzymes that influence flux through fatty-acid oxidation and oxidative phosphorylation pathways in high-altitude deer mice and by concomitant changes in the expression of genes in these same pathways. Contrary to predictions derived from studies of humans at high altitude, our results suggest that selection to sustain prolonged thermogenesis under hypoxia promotes a shift in metabolic fuel use in favor of lipids over carbohydrates.functional genomics | RNA-seq | thermoregulation | transcriptomics D uring cold stress, homeothermic endotherms maintain a constant body temperature by increasing metabolic heat production. In small endotherms like mice that have high thermoregulatory demands, thermogenic capacity influences survival in cold environments and therefore has a clear connection to Darwinian fitness (1, 2). Indeed, thermogenic capacity in freeranging deer mice (Peromyscus maniculatus) is subject to strong directional selection at high altitude (3).Sustaining maximal thermogenic capacities during prolonged periods of cold stress requires a high rate of O 2 flux through oxidative pathways, and this requirement presents a unique challenge for endothermic animals that live under conditions of chronic O 2 deprivation at high altitude. The reduced partial pressure of O 2 (PO 2 ) at high altitude imposes well-documented constraints on aerobic metabolism (4-8), thereby exacerbating the increased thermoregulatory demands faced by endothermic animals that are native to cold, alpine environments.In rodents, aerobic thermogenesis is accomplished through both shivering and nonshivering mechanisms, and in deer mice, shivering accounts for roughly 35-50% of total thermogenic capacity (9). As with other forms of strenuous exerci...

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Section: Resultsmentioning

confidence: 94%

Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice

Cheviron

Bachman

Connaty

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

168

226

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“…This species breeds on the high plateaus of central Asia and, remarkably, has been observed flying over the summit of Mt Everest (8850 m) during its fall migration to northeastern India (Swan, 1970). A number of physiological traits increase O 2 uptake, circulation and diffusion to contribute to the remarkable physiological performance of bar-headed geese in hypoxic conditions (Petschow et al, 1977;Perutz, 1983;Jessen et al, 1991;Scott and Milsom, 2007;Scott et al, 2009aScott et al, , b, 2011. Recently, Scott et al (2011) reported variation in cytochrome c oxidase (COX) enzyme kinetics between bar-headed geese and closely related lowland species.…”

Section: Hb Polymorphisms In Deer Micementioning

confidence: 99%

Genomic insights into adaptation to high-altitude environments

2011

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Elucidating the molecular genetic basis of adaptive traits is a central goal of evolutionary genetics. The cold, hypoxic conditions of high-altitude habitats impose severe metabolic demands on endothermic vertebrates, and understanding how high-altitude endotherms cope with the combined effects of hypoxia and cold can provide important insights into the process of adaptive evolution. The physiological responses to high-altitude stress have been the subject of over a century of research, and recent advances in genomic technologies have opened up exciting opportunities to explore the molecular genetic basis of adaptive physiological traits. Here, we review recent literature on the use of genomic approaches to study adaptation to high-altitude hypoxia in terrestrial vertebrates, and explore opportunities provided by newly developed technologies to address unanswered questions in high-altitude adaptation at a genomic scale.

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“…Incredibly, bar-headed geese sustain the 10 -20-fold increase in O 2 consumption rate that is necessary to fuel flapping flight (Ward et al 2002), despite the severe hypoxia at these elevations. The physiological basis for this elevated O 2 transport capacity is not completely understood, but it results in part from evolutionary changes that improve O 2 uptake and circulation during hypoxia (Petschow et al 1977;Jessen et al 1991;Scott & Milsom 2007). Much less is known about the flight muscle of this species, but theoretical modelling suggests that an enhanced capacity for O 2 diffusion from blood into muscle, which can be realized with increased muscle capillarity, should also improve O 2 transport in hypoxia (Scott & Milsom 2006).…”

Section: Introductionmentioning

confidence: 99%

Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose

et al. 2009

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Bar-headed geese migrate over the Himalayas at up to 9000 m elevation, but it is unclear how they sustain the high metabolic rates needed for flight in the severe hypoxia at these altitudes. To better understand the basis for this physiological feat, we compared the flight muscle phenotype of bar-headed geese with that of low altitude birds (barnacle geese, pink-footed geese, greylag geese and mallard ducks). Bar-headed goose muscle had a higher proportion of oxidative fibres. This increased muscle aerobic capacity, because the mitochondrial volume densities of each fibre type were similar between species. However, bar-headed geese had more capillaries per muscle fibre than expected from this increase in aerobic capacity, as well as higher capillary densities and more homogeneous capillary spacing. Their mitochondria were also redistributed towards the subsarcolemma (cell membrane) and adjacent to capillaries. These alterations should improve O 2 diffusion capacity from the blood and reduce intracellular O 2 diffusion distances, respectively. The unique differences in bar-headed geese were much greater than the minor variation between low altitude species and existed without prior exercise or hypoxia exposure, and the correlation of these traits to flight altitude was independent of phylogeny. In contrast, isolated mitochondria had similar respiratory capacities, O 2 kinetics and phosphorylation efficiencies across species. Bar-headed geese have therefore evolved for exercise in hypoxia by enhancing the O 2 supply to flight muscle.

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Control of breathing and adaptation to high altitude in the bar-headed goose

Cited by 96 publications

References 62 publications

Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice

Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice

Genomic insights into adaptation to high-altitude environments

Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose

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